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What makes Grande1 retrotransposon different?

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Abstract

Grande1 elements constitute a family of Ty3 retrotransposons present in the Zea genus in more than 1000 copies in Zea diploperennis and maize. The sequences of three Grande1 flanking regions, two from Z. diploperennis and one from maize, reveal transposable elements as insertion targets, suggesting a preferential integration of Grande1 elements into other transposable elements. These retrotransposons are remarkable for their large size of around 14 kb, which is a consequence of a very large 3′ region of more than 7 kb. Atypical entities within this region are two arrays of unrelated tandem repeats with potential stable stem-loop structures. A large portion of the same region is occupied by ORFs, although only ORF23, whose function is unknown, is presumably transcribed in antisense orientation to the reverse transcriptase ORF. Only ORF23 has a codon usage similar to the one tabulated for highly-expressed maize genes. Correspondingly, the transcript of 900 b that hybridizes with ORF23 probes is found in all the maize tissues explored. This is despite the high level of methylation in the DNA of Grande1. Genomic RNA has not been detected in any tissue or situation studied, probably reflecting a non-functional retrotransposon. The origin of ORF23 and the remainder 3′ region might be due to a transduction event.

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References

  • Aksoy, S., S. Williams, S. Chang & F.F. Richards, 1990. SLACS retrotransposon from Tripanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res. 18: 785–792.

    PubMed  CAS  Google Scholar 

  • Aledo, R., R. Raz, A. Monfort, C.M. Vicient, P. Puigdomenech & J. A. Martinez-Izquierdo, 1995. Chromosome Localization and characterization of a family of long interspersed repetitive DNA elements from the genus Zea. Theor. Appl. Genet. 90: 1094–1100.

    Article  CAS  Google Scholar 

  • Arumuganathan, K. & E.D. Earle, 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208–218.

    CAS  Google Scholar 

  • Bennetzen, J.L., 1996. The contributions of retroelements to plant genome organization, function and evolution. Trends Microbiol. 4: 347–353.

    Article  PubMed  CAS  Google Scholar 

  • Boeke, J.D. & V.G. Corces, 1989. Transcription and reverse tran-scription of retrotransposons. Annu. Rev. Microbiol. 42: 403–434.

    Article  Google Scholar 

  • Bureau, T.E. & S.R. Wessler, 1992. Tourist: a large family of small inverted repeat elements frequently associated with maize genes. Plant Cell 4: 1283–1294.

    Article  PubMed  CAS  Google Scholar 

  • Bureau, T.E. & S.R. Wessler, 1994. Mobile inverted-repeat elements of the tourist family are associated with the genes of many cereal grasses. Proc. Natl. Acad. Sci. USA 91: 1411–1415.

    Article  PubMed  CAS  Google Scholar 

  • Bureau, T.E., S.E. White & S.R. Wessler, 1994. Transduction of a cellular gene by plant retroelement. Cell 77: 479–480.

    Article  PubMed  CAS  Google Scholar 

  • Chavanne, F., D.X. Zhang, M.F. Liaud & R. Cerff, 1994. Structure and evolution of a new gypsy-like retrotransposon in pea (Tps1). Abstract 203. 4th International Congress of Plant Molecular Biol-ogy. Amsterdam.

  • Day, A. & J.D. Rochaix, 1991. Structure and Inheritance of sense and anti-sense transcripts from a transposon in the green alga Chlamydomonas reinhardtii. J. Mol. Biol. 218: 273–291.

    Article  PubMed  CAS  Google Scholar 

  • Day, A., M. Schirmer-Rahire, M.R. Kuchka, S.P. Mayfield & J-D. Rochaix, 1988. Atransposon with an unusual arrangement of long terminal repeats in the green alga Chlamydomonas reinhardtii. EMBO J. 7: 1917–1927.

    PubMed  CAS  Google Scholar 

  • Dellaporta, S.L., J. Wood & J.B. Hicks, 1983. A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1: 19–21.

    CAS  Google Scholar 

  • Devereux, J., P. Haeberli & O. Smithies, 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387–395.

    PubMed  CAS  Google Scholar 

  • Fedoroff, N.V., 1989. About maize transposable elements and devel-opment. Cell 56: 181–191.

    Article  PubMed  CAS  Google Scholar 

  • Fickett, J.W., 1982. Recognition of protein coding regions in DNA sequences. Nucleic Acids Res. 10: 5303–5318.

    PubMed  CAS  Google Scholar 

  • Finnegan, E.J., R.I.S. Brettell & E.S. Dennis, 1993. The role of DNA methylation in the regulation of plant gene expression, pp. 218–261 in DNA Methylation: Molecular Biology and Biological Significance, edited by J.P. Jost and H.P. Saluz. Birkhauser Verlag, Basle, Switzerland.

    Google Scholar 

  • Flavell, A.J., 1992. Ty1-copia group retrotransposons and the evolu-tion of retroelements in the eukaryotes. Genetica 86: 203–214.

    Article  PubMed  CAS  Google Scholar 

  • Flavell, R.B., M. O'Dell & W.F. Thompson, 1988. Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J. Mol. Biol. 204: 523–534.

    Article  PubMed  CAS  Google Scholar 

  • Grasser, K.D., 1995. Plant chromosomal high mobility group (HMG) proteins. Plant J. 7: 185–192.

    Article  PubMed  CAS  Google Scholar 

  • Gruenbaum, Y., T. Naveh-Many, H. Cedar & A. Razin, 1981. Sequence specificity of methylation in higher plant DNA. Nature 292: 860–862.

    Article  PubMed  CAS  Google Scholar 

  • Hershberger, R.J., M.I. Benito, K.J. Hardeman, C. Warren, V.L. Chandler & V. Walbot, 1995. Characterization of the major tran-.27 scripts encoded by the regulatory MuDR transposable element in maize. Genetics 140: 1087–1098.

    PubMed  CAS  Google Scholar 

  • Higgins, D.G., A.J. Bleasby & R. Fuchs, 1992. CLUSTAL V: improved software for multiple sequence alignment. CABIOS 8: 189–191.

    PubMed  CAS  Google Scholar 

  • Hu, W., O.P. Das & J. Messing, 1995. Zeon-1, a member of a new maize retrotransposon family. Mol. Gen. Genet. 248: 471–480.

    Article  PubMed  CAS  Google Scholar 

  • Huijser, P., C. Kirchhoff, D.H. Lankenau & W. Hennig, 1988. Retrotransposon-like sequences are expressed in Y chromoso-mal lampbrush loops of Drosophila hydei. J. Mol. Biol. 203: 689–697.

    Article  PubMed  CAS  Google Scholar 

  • Ilyin, Y.V., N.V. Lyubomirskaya & A.I. Kim, 1991. Retrotransposon gypsy and genetic instability in Drosophila. Genetica 85: 13–22.

    Article  PubMed  CAS  Google Scholar 

  • James, M.G., M.J. Scanlon, M. Qin, D.S. Robertson & A.M. Myers, 1993. DNAsequence and transcript analysis of transposon MuA2, a regulator of Mutator transposable element activity in maize. Plant Mol. Biol. 21: 1181–1185.

    Article  PubMed  CAS  Google Scholar 

  • Jin, Y.K. & J.L. Bennetzen, 1994. Integration and nonrandom muta-tion of a plasma membrane proton ATPase gene fragment within Bs1 retroelement of maize. Plant Cell 6: 1177–1186.

    Article  PubMed  CAS  Google Scholar 

  • Kim, A., C. Terzian, P. Santamar´ýa, A. Pelisson, N. Prud'Homme & A. Bucheton, 1994. Retroviruses in invertebrates: the gypsy retro-transposon is apparently an infectious retrovirus of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 91: 1285–1289.

    Article  PubMed  CAS  Google Scholar 

  • Kleckner, N., 1989. Transposon Tn10, pp. 227–268 in Mobile DNA, edited by D. E. Berg and M.M. Howe. Am. Soc. Microbiol. Washington, DC.

  • Kozak, M., 1984. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 12: 857–872.

    PubMed  CAS  Google Scholar 

  • Labrador, M. & A. Fontdevila, 1994. High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon. Mol. Gen. Genet. 245: 661–674.

    Article  PubMed  CAS  Google Scholar 

  • Lankenau, D.H., 1993. The retrotransposon family micropia in Drosophila species, pp. 232–241 in Transposable Elements and Evolution, edited by J.F. McDonald. Kluwer Academic Publish-ers, Netherlands.

    Google Scholar 

  • Lankenau, S., V.G. Corces & D.H. Lankenau, 1994. The Drosophila micropia retrotransposon encodes a testis specific antisense RNA complementary to reverse transcriptase. Mol. Cell. Biol. 14: 1764–1775.

    PubMed  CAS  Google Scholar 

  • Lloyd, J.A. & S.S. Potter, 1988. Distinct subfamilies of primate LiGg retroposons, with some elements carrying tandem repeats in the 50 region. Nucleic Acids Res. 16: 6147–6156.

    PubMed  CAS  Google Scholar 

  • Loeb, D.D., R.W. Padgett, S.C. Hardies, W.R. Shehee, M.B. Comer, M.H. Edgell & C.A. Hutchison, III, 1986. The sequence of a large L1Md element reveals a tandemly repeated 50 end and several features found in retrotransposons. Mol. Cell. Biol. 6: 168–182.

    PubMed  CAS  Google Scholar 

  • Logemann, J., J. Schell & L. Willmitzer, 1987. Improved method for the isolation of RNA from plat tissues. Ann. Biochem. 163: 16–20.

    Article  CAS  Google Scholar 

  • Lucas, H., G. Moore, G. Murphy & R.B. Flavell, 1992. Inverted repeats in the long-terminal repeats of the wheat retrotransposon Wis 2–1 A. Mol. Biol. Evol. 9: 716–728.

    PubMed  CAS  Google Scholar 

  • Manninen, I. & A.H. Schulman, 1993. BARE-1, a copia-like retroelement in barley (Hordeum vulgare L.). Plant Mol. Biol. 22: 829–846.

    Article  PubMed  CAS  Google Scholar 

  • McMullen, M.D., B. Hunter, R.L. Phillips & I. Rubenstein, 1986. The structure of the maize ribosomal DNA spacer region. NucleicAcid Res. 14: 4953–4969.

    Article  CAS  Google Scholar 

  • Monfort, A., C.M. Vicient, R. Raz, P. Puigdomenech & J.A. Martínez-Izquierdo, 1995. Molecular analysis of a putative trans-posable retroelement from the Zea genus with internal clusters of tandem repeats. DNA Res. 2: 255–261.

    Article  PubMed  CAS  Google Scholar 

  • Moore, G., H. Lucas, N. Batty & R.A. Flavell, 1991. A family of retrotransposons and associated genomic variation in wheat. Genomics 10: 461–468.

    Article  PubMed  CAS  Google Scholar 

  • Ohtsubo, H. & E. Ohtsubo, 1994. Involvement of transposition in dispersion of tandem repeat sequences (TrsA) in rice genomes. Mol. Gen. Genet. 245: 449–455.

    Article  PubMed  CAS  Google Scholar 

  • Pelissier, T., S. Tutois, J.M. Deragon, S. Tourmente, S. Genestier & G. Picard, 1995. Athila, a new retroelement from Arabidopsis thaliana. Plant Mol. Biol. 29: 441–452.

    Article  PubMed  CAS  Google Scholar 

  • Prat, S., J. Cortadas, P. Puigdomènech & J. Palau, 1985. Nucleic acid (cDNA) and amino acid sequences of the endosperm protein glutelin-2. Nucleic Acids Res. 13: 1493–1504.

    PubMed  CAS  Google Scholar 

  • Proudfoot, N.J., 1989. HowRNApolymerase II terminates transcrip-tion in higher eukaryotes. Trends Biochem. Sci. 14: 105–110.

    Article  PubMed  CAS  Google Scholar 

  • Raz, R., P. Puigdomenech & J.A. Mart´ýnez-Izquierdo, 1991. A new family of repetitive nucleotide sequences is restricted to the genus Zea. Gene 105: 151–158.

    Article  PubMed  CAS  Google Scholar 

  • Rothnie, H.M., K.J. McCurrach, L.A. Glover & N. Hardman, 1990. Retrotransposon-like nature of Tp1 elements: implications for the organization of highly repetitive, hypermethylated DNA in the genome ofPhysarum polycephalum. Nucleic Acids Res. 19: 279–286.

    Google Scholar 

  • Saitou, N. & N. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    PubMed  CAS  Google Scholar 

  • Sambrook, J., E.F. Fritsch & T. Maniatis, 1989. Molecular Cloning:a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.

    Google Scholar 

  • Sandmeyer, S. B., L. J. Hansen & D. L. Chalker, 1990. Integra-tion specificity of retrotransposons and retroviruses. Annu. Rev.Genet. 24: 491–518.

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel, P., A. Tikhonov, Y-K. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer, K.J. Edwards, M. Lee, Z. Avramova & J.L. Bennetzen, 1996. Nested retrotrans-posons in the intergenic regions of the maize genome. Science 274: 765–768.

    Article  PubMed  CAS  Google Scholar 

  • Scheineker, V.S., E.R. Lozovskaya, J.G. Bishop & M.B. Evgen'ev,1990. A long terminal repeat-containing retrotransposon is mobi-lized during hybrid dysgenesis in Drosophila virilis. Proc. Natl. Acad. Sci. USA 87: 9615–9619.

    Article  Google Scholar 

  • Schwarz-Sommer, Z. & H. Saedler, 1988. Transposons and retro-transposons in plants: analysis and biological relevance, pp. 343–354 in Transposition, edited by A.J. Kingsman, K.F. Chater and S.M. Kingsman. The Society for General Microbiology, Sympo-sium 43. Cambridge University Press, UK.

    Google Scholar 

  • Selker, E.U., 1990. DNA methylation and chromatin structure: a view from below. Trends Biochem. Sci. 15: 103–107.

    Article  PubMed  CAS  Google Scholar 

  • Sentry, J.W. & D.R. Smyth, 1989. An element with long terminal repeats and its variant arrangements in the genome of Lilium henryi. Mol. Gen. Genet. 215: 349–354.

    Article  PubMed  CAS  Google Scholar 

  • Severynse, D.M., C.A. Hutchinson & M.H. Edgell, 1992. Identifi-cation of transcriptional regulatory activity within the 50 A-type monomer sequence of the mouse LINE-1 retroposon. Mamm. Genome 2: 41–50.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd, N.S., Z. Schwarz-Sommer, J. Blumnerg vel Spalve, M. Gupta, U. Wienand & H. Saedler, 1984. Similarity of the Cin1 repetitive family of Zea mays to eukaryotic transposable ele-ments. Nature 307: 185–187.

    Article  PubMed  CAS  Google Scholar 

  • Smyth, D.R., P. Kalitsis, J.L. Jospeh & J.W. Sentry, 1989. Plant retrotransposon from Lilium henryi is related to Ty3 of yeast and the gypsy group of Drosophila. Proc. Natl. Acad. Sci. USA 86: 5015–5019

    Article  PubMed  CAS  Google Scholar 

  • Varmus, H. & P. Brown, 1989. Retroviruses, pp. 53–108 in Mobile DNA, edited by D.E. Berg and M.M. Howe. Am. Soc. Microbiol.Washington, DC.

  • Vicient, C.M. Caracterizaci´ on molecular de Grande1, un nuevo retrotranspos´ on del g´ enero Zea. Ph.D. Thesis, University of Barcelona, Spain, 1995.

    Google Scholar 

  • Vicient, C.M. & J.A. Mart´ýnez-Izquierdo, 1997. Discovery of a Zdel transposable element in Zea species as a consequence of a retrotransposon insertion. Gene 184: 257–261.

    Article  PubMed  CAS  Google Scholar 

  • Weiner, A.M. & R.A. Denison, 1982. Either gene amplification or gene conversion may maintain the homogeneity of the multigene family encoding human U1 small nuclear RNA. Cold Spring Harbor Symp. Quant. Biol. 47: 1141–1149.

    CAS  Google Scholar 

  • White, S.E., L.F. Habera & S.R. Wessler, 1994. Retrotransposons in the flanking regions of normal plant genes: a role for copia-like elements in the evolution of gene structure and expression. Proc. Natl. Acad. Sci. USA 91: 11792–11796.

    Article  PubMed  CAS  Google Scholar 

  • Woerner, A.M. & C.J. Marcus-Sekura, 1993. Characterization of a DNA binding domain in the C-terminus of HIV-1 integrase by deletion mutagenesis. Nucleic Acids Res. 21: 3507–3511.

    PubMed  CAS  Google Scholar 

  • Xiong, S., W.D. Burke & T.H. Eickbush, 1993. Pao, a highly retro-transposable element from Bombyx mori containing long termi-nal repeats with tandem copies of the putative R region. Nucleic Acids Res. 21: 2117–2123.

    PubMed  CAS  Google Scholar 

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Martínez-Izquierdo, J.A., García-Martínez, J. & Vicient, C.M. What makes Grande1 retrotransposon different?. Genetica 100, 15–28 (1997). https://doi.org/10.1023/A:1018332218319

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